ArticleCell stem cell2023
Development of functional resident macrophages in human pluripotent stem cell-derived colonic organoids and human fetal colon.
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Article in Cell stem cell, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 47 papers.
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47citing papers in PubMed
9.4field-weighted citation impact, top 2% of its field
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Who cites it
47 citing papers in PubMed, 57 citations in OpenAlex.
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- Macrophage heterogeneity in human secondary lymphoid organs.Clinical science (London, England : 1979) · 2026Review
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- Substrate pre-stretch reprograms macrophage behavior through surface topographical remodeling.Mechanobiology in medicine · 2026Article
- Macrophages orchestrate antiviral defense and epithelial repair in a human iPSC-derived alveolar air-liquid interface.JCI insight · 2026Article
- Review
- Generation of biologically responsive colon-like intestinal tissue patches from human induced pluripotent stem cells using a rapid co-differentiation platform.Stem cell research & therapy · 2026Article
- Single-cell transcriptomic comparison of the developing human fetal stomach and pluripotent stem cell-derived gastric organoids.Development (Cambridge, England) · 2026Article
- Development and Transformation of Veterinary Experimental In Vitro Models: From 2D Culture to 3D Organoids.Animals : an open access journal from MDPI · 2026Review
- A Scalable Organoid Model of Urothelial Aging for Metabolic Interrogation, Infection Modeling, and Reversal of Age-Associated Changes.Aging cell · 2026Article
- Advances and continuing challenges in differentiation of stem cells to human kidney tissue.Nature reviews. Nephrology · 2026Review
- Peptide-functionalized membrane camouflage for endogenous HNature communications · 2026Article
- Highly Efficient Derivation of Functional Human-Induced Pluripotent Stem Cell-Derived Macrophages under Serum-Free Conditions to Study Innate Immune Responses.Journal of innate immunity · 2026Article
- Oxygen-enhanced assembloid-based vascularized intestinal-on-a-chip for radioprotective drug evaluation.Frontiers in toxicology · 2026Article
- Hidden in Plain Sight: Alphavirus Persistence and Its Potential for Driving Chronic Pathogenesis.Viruses · 2025Review
- Single-cell sequencing and organoids: applications in organ development and disease.Molecular biomedicine · 2025Review
- Immune and Immune-Integrated Organoids as NextGeneration Platforms for Disease Modeling.MedComm · 2025Review
- Urine-derived stem cells efficiently assemble into micro-bone organoids supported by decellularized bone matrix microparticles for rapidly repairing bone defects through direct filling and paracrine functions.Materials today. Bio · 2025Article
- Temporal Regulation of Cytokines and Growth Factors for Optimized Hematopoietic-Lineage Specification from Human Pluripotent Stem Cells.International journal of stem cells · 2025Article
- Conserved interactions with stromal and immune cells coordinate de novo B cell lymphopoiesis in fetal intestines.JCI insight · 2025Article
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Authors and funding
29 authors at 6 institutions in 1 country.
Jorge O MúneraDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA; Department of Regenerative Medicine and Cell Biology, Medical University of South Carolina, Charleston, SC 29425, USA. Electronic address: munera@musc.edu.
Daniel O KecheleDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Carine BouffiDivision of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Na QuDepartment of Regenerative Medicine and Cell Biology, Medical University of South Carolina, Charleston, SC 29425, USA.
Ran JingStem Cell Program, Boston Children's Hospital, Boston, MA, USA; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USA.
Pritiprasanna MaityDepartment of Regenerative Medicine and Cell Biology, Medical University of South Carolina, Charleston, SC 29425, USA.
Jacob R EnriquezDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Lu HanDepartment of Biochemistry and Molecular Biology, Hollings Cancer Center, Medical University of South Carolina, Charleston, SC, USA.
Ian CampbellDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Maxime M MaheDivision of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Heather A McCauleyDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Xinghao ZhangDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Nambirajan SundaramDivision of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Jonathan R HudsonDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Adrian Zarsozo-LacosteDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Suman PradhanDepartment of Molecular and Cellular Physiology, University of Cincinnati, Cincinnati, OH 45267, USA.
Kentaro TominagaDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
J Guillermo SanchezDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Alison A WeissDepartment of Molecular and Cellular Physiology, University of Cincinnati, Cincinnati, OH 45267, USA.
Praneet ChatuvediDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA.
Jason R SpenceDivision of Gastroenterology and Hepatology, Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
Mariam HachimiStem Cell Program, Boston Children's Hospital, Boston, MA, USA.
Trista NorthStem Cell Program, Boston Children's Hospital, Boston, MA, USA.
George Q DaleyStem Cell Program, Boston Children's Hospital, Boston, MA, USA; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USA.
Christopher N MayhewDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA; Pluripotent Stem Cell Facility, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Yueh-Chiang HuDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA; Pluripotent Stem Cell Facility, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Takanori TakebeDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA; Center for Stem Cell and Organoid Medicine (CuSTOM), Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Michael A HelmrathDivision of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA; Center for Stem Cell and Organoid Medicine (CuSTOM), Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
James M WellsDivision of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH 45229-3039, USA; Center for Stem Cell and Organoid Medicine (CuSTOM), Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA; Division of Endocrinology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA. Electronic address: james.wells@cchmc.org.
Cincinnati Children's Hospital Medical Center · USMedical University of South Carolina · USBoston Children's Hospital · USUniversity of Cincinnati · USHarvard University · USUniversity of Michigan–Ann Arbor · US
Funding
Stem Cell/Organoid and Genome Editing CoreP30DK078392 · NIDDK · CINCINNATI CHILDRENS HOSP MED CTR · PI Alexander Miethke · 2007 to 2026
$24.4MThe role of SMAD1 and SATB2 in colon patterningP20GM130457 · NIGMS · MEDICAL UNIVERSITY OF SOUTH CAROLINA · PI Hailong Zhang · 2020 to 2026
$18.7MProject-3: Modeling EA/TEF in human organoidsP01HD093363 · NICHD · CINCINNATI CHILDRENS HOSP MED CTR · PI Wendy K Chung, Paul scot Kingma · 2017 to 2026
$16.2MENVIRONMETAL CARCINOGENESIS AND MUTAGENESIST32ES007250 · NIEHS · UNIVERSITY OF CINCINNATI · PI MILLER, WILLIAM E · 1988 to 2024
$11.9MProteomics CoreP30DK123704 · NIDDK · MEDICAL UNIVERSITY OF SOUTH CAROLINA · PI DON C. ROCKEY · 2020 to 2026
$8.8MMolecular Circuits in the Hematopoietic Stem Cell NicheRC2DK120535 · NIDDK · BOSTON CHILDREN'S HOSPITAL · PI COLLINS, JAMES J, DALEY, GEORGE Q · 2020 to 2024
$8.2MModeling diabetes using an integrated plate systemUH3DK119982 · NIDDK · CINCINNATI CHILDRENS HOSP MED CTR · PI LEE, MOO-YEAL, WELLS, JAMES M · 2020 to 2022
$5.4MOrganoids as a Model System for Studying Gastrointestinal DiseaseU19AI116491 · NIAID · UNIVERSITY OF CINCINNATI · PI WELLS, JAMES M · 2015 to 2019
$4.6MInvestigation of Regional Identity in Human Intestinal Stem CellsU01DK103117 · NIDDK · CINCINNATI CHILDRENS HOSP MED CTR · PI HELMRATH, MICHAEL A. · 2014 to 2023
$4.0MModeling diabetes using an integrated plate systemUG3DK119982 · NIDDK · CINCINNATI CHILDRENS HOSP MED CTR · PI LEE, MOO-YEAL, WELLS, JAMES M · 2018 to 2019
$1.7MHuman iPSC intestine mimetics with integrated mesenchymal, endothelial and enteric nervous tissueR01DK137806 · NIDDK · UNIVERSITY OF MICHIGAN AT ANN ARBOR · PI Jason Spence · 2024 to 2026
$1.5MEstablishment of in vitro and in vivo models of human gastrointestinal organoids with a functional ENSU18EB021780 · NIBIB · CINCINNATI CHILDRENS HOSP MED CTR · PI HELMRATH, MICHAEL A., WELLS, JAMES M · 2015 to 2016
$622kNIAID NIH HHS U19 AI116491NIBIB NIH HHS U18 EB021780NICHD NIH HHS P01 HD093363NIDDK NIH HHS P30 DK078392NIDDK NIH HHS P30 DK123704NIDDK NIH HHS R01 DK137806NIDDK NIH HHS RC2 DK120535NIDDK NIH HHS U01 DK103117NIDDK NIH HHS UG3 DK119982NIDDK NIH HHS UH3 DK119982NIEHS NIH HHS T32 ES007250NIGMS NIH HHS P20 GM130457
Abstract
Most organs have tissue-resident immune cells. Human organoids lack these immune cells, which limits their utility in modeling many normal and disease processes. Here, we describe that pluripotent stem cell-derived human colonic organoids (HCOs) co-develop a diverse population of immune cells, including hemogenic endothelium (HE)-like cells and erythromyeloid progenitors that undergo stereotypical steps in differentiation, resulting in the generation of functional macrophages. HCO macrophages acquired a transcriptional signature resembling human fetal small and large intestine tissue-resident macrophages. HCO macrophages modulate cytokine secretion in response to pro- and anti-inflammatory signals and were able to phagocytose and mount a robust response to pathogenic bacteria. When transplanted into mice, HCO macrophages were maintained within the colonic organoid tissue, established a close association with the colonic epithelium, and were not displaced by the host bone-marrow-derived macrophages. These studies suggest that HE in HCOs gives rise to multipotent hematopoietic progenitors and functional tissue-resident macrophages.
Indexed as
Pluripotent Stem CellsAnimalsColonHematopoietic Stem CellsHumansMacrophagesMiceOrganoidsendothelial-to-hematopoietic transitionhemogenic endotheliumhuman colonic organoidstissue-resident macrophages
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